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Mountain Pine Beetle Mutualist Leptographium Longiclavatum Presence in the Southern Rocky Mountains During a Record Warm Period

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Mountain Pine Beetle Mutualist Leptographium Longiclavatum Presence in the Southern Rocky Mountains During a Record Warm Period DOI 10.12905/0380.sydowia70-2018-0001 Published online 30 April 2018 Mountain pine beetle mutualist Leptographium longiclavatum presence in the southern Rocky Mountains during a record warm period Javier E. Mercado1,* & Beatriz Ortiz-Santana2 1 Rocky Mountain Research Station, 240 W Prospect Rd., Fort Collins, CO 80526 2 Northern Research Station, One Gifford Pinchot Dr., Madison, WI 53726 * e-mail: [email protected] Mercado J.E. & Ortiz-Santana B. (2018) Mountain pine beetle mutualist Leptographium longiclavatum presence in the south- ern Rocky Mountains during a record warm period. – Sydowia 70: 1–10. We studied blue-stain fungi (Ophiostomataceae: Ophiostomatales) of mountain pine beetle in declining epidemic populations affecting three pine species in Colorado. Using morphological and molecular characterizations, we determined the presence of the mutualist L. longiclavatum in the southern Rocky Mountains of Colorado, where it was as common as the warm temperature adapted O. montium within the insect’s specialized maxillary mycangium. The species was more prevalent than its “sibling spe- cies” G. clavigera which is the the common mycangial mutualist documented in USA populations. Findings were made during a two-year period including the warmest year on record in the state (i. e., 2012). Other studies have indicated that L. longiclavatum is more frequent in insect populations occurring in the northern Canadian Rockies diminishing in southern areas of that moun- tain range, suggesting latitude influences the frequency of this fungal mutualists, due to its better cool temperature tolerances. Our findings suggest Colorado isolates may have a greater tolerance of warmer temperatures than those from the north. These findings also increase our knowledge about the species distribution and the in situ conditions permissive of its occurrence in areas south of the Canadian Rockies. Keywords: blue-stain, mycangia, mutualist, symbiont, phytopathogen. Populations of mountain pine beetle (Dendroc- Fengel 1988, 1990). The relationship between MPB tonus ponderosae), hereafter MPB, have been in an and its three main fungal associates Grosmannia irruptive stage across many western North Ameri- clavigera (Rob.-Jeffr. & R.W. Davidson) Zipfel, Z.W. can pine forests since the 1990s. Since then, out- de Beer & M.J. Wingf., Leptographium longiclava- breaks have spread to unusually high latitudes in tum S.W. Lee, J.J. Kim & C. Breuil, and Ophiostoma Canada including new areas in Alberta (Culling- montium (Rumbold) Arx represents a near obligate ham et al. 2011). Populations have also reached un- mutualistic symbiosis in which these fungi obtain usually high elevations in the Rocky Mountains. In transport mainly by the MPB. Similarly, the beetle’s northern Colorado, attacks by the MPB at eleva- larvae require nutrients from the beneficial blue- tions higher than 3000 m are not common and have stain fungi to fully develop into adults (Six & Paine been discussed only in one internal report (DeLeon 1998, Myrholm & Langor 2015). 1939, unpubl.) and a single publication (Mitton & Across the USA, the occurrence of the MPB sym- Ferrenberg 2012). These expansions may be attrib- bionts G. clavigera and O. montium has been docu- uted to a warming climate. mented for several decades (Rumbold 1941, Robin- Bark beetles can carry a wide range of phoretic son-Jeffrey & Davidson 1968). However, L. longi- associates (Mercado et al. 2014, Hofstetter et al. clavatum has only recently been documented from 2015) including important mutualists that may also continental USA, first in California (Lee et al. 2005, become affected by changes in climate. Of these, the Massoumi Alamouti et al. 2011) and later from most best understood are the ophiostomatoid blue-stain of the states where the MPB occurs (Ojeda Alayon fungi. The name “blue-stain fungi” comes from the et al. 2017). The species has been frequently report- characteristic grayish blue-green hues seen on in- ed from MPB populations in Canada (Lee et al. fected wood due to refraction of incident natural 2005, Rice et al. 2008, Roe et al. 2011, among others). light by the melanin in their hyphal bodies (Zink & A caveat of previous knowledge from the USA is Sydowia 70 (2018) 1 Mercado & Ortiz-Santana: Beetle mutualist Leptographium longiclavatum that investigations utilizing techniques capable of ing familiarized, amended media was not used for detecting this MPB fungal symbiont in the US have the rest of the study to obtain information about been used less frequently than in Canada (Ojeda other MPB fungal associates for future studies. Alayon et al. 2017). Our objective was to determine Direct cultures of dissected mycangia and ely- the main blue-stain fungal species of MPB popula- tral surfaces were grown in un-amended 2 % MEA tions affecting areas of three common host pines in petri dishes (100 mm). A direct culture method of northern Colorado, using morphological and mo- specific transporting structures of the MPB was lecular characterizations. chosen following previous studies (Whitney & Far- ris 1970, Six & Paine 1998). Within two to seven Materials and methods days after initial culture, agar plugs (2 mm) of mor- phologically different fungi were transferred to wa- Field sampling ter agar. Two to four days later, hyphal tips were To infer potential effects of temperature in blue- transferred to un-amended 2 % MEA plates to grow stain fungi diversity we instrumented trees with pure fungal strains. Colonies were grown at room temperature sensors (Onset, S-TMB-M002) in 2011 temperature (22 °C) without protection from day- and within 5 days of insect attacks to measure phlo- time fluorescent light exposure for a period of 28 em temperatures during their development. These days. Replicates of pure fungal cultures were used probes were drilled into the phloem at the north for DNA extraction and to study fungal growth and south sides. In 2012 and 2013, adult flying MPB characters in wood discs. Conidia were produced were collected at different sites in the Roosevelt profusely in sterile wood discs from the MPB three National Forest in northern Colorado from a popu- pine hosts; therefore, these were used to examine lation receding from the climax of its epidemic in the type of conidia and conidiophore as well. 2011 (Figs. 1–2). Insect collections were made dur- ing mid to late July which corresponded to the bee- Morphological determinations tle’s main flight and attack period during these Observed cultural characters used to distinguish years. Bark beetles were not directly handled nor L. longiclavatum from G. clavigera were those de- did these interact with other insects as these were scribed by Lee et al. (2005). Characters used to de- induced to drop into individual sterile micro centri- termine O. montium were those defined by Rumbold fuge tubes with lid (1.5 ml, Fisher Scientific). In- (1941). Microscopic characterization using the sects were transported in coolers and refrigerated Stereomaster (Fisher Scientific) and Eclipse TS100 at the laboratory at –18 °C until processed. (Nikon) microscopes included distinguishing the asexual morphs Hyalorhinocladiella from Lep- Statistical analyses on fungal presence tographium, as well as the types of conidia pro- We compared prevalence (a proportion) which duced by the fungi. inherently accounts for differences in the number of MPBs obtained across years. We used a generalized Molecular determinations linear mixed model (GLMM) with a logit link to as- DNA sequences of the nuclear ribosomal ITS2- sess patterns in fungal presence and included MPB LSU (partial 5.8 + ITS 2 + partial 28S) and the pro- ID as a random effect to account for repeated obser- tein-coding gene β-tubulin (partial gene) were used vations (Hosmer et al. 2013). Differences between in the present study. DNA extraction and amplifica- factors (year and species) were discerned using Tuk- tion were performed at the Center for Forest Mycol- ey multiple comparisons. All statistical analyses ogy Research (CFMR) while the sequencing was per- were performed in R using the lme4 and multcomp formed at the University of Wisconsin Biotechnology packages (Hothorn et al. 2008, R Core Team 2017). Center (UWBC) in Madison, WI. DNA was extracted with a CTAB protocol following Palmer et al. (2008) Fungal culturing and Lorch et al. (2013), but with certain modifica- In 2011, the first author became familiar with tions. A small amount of mycelium from cultures the blue-stain fungi transported by the mountain was scraped using a flattened inoculation needle and pine beetle in Colorado. At first, the protocol used placed in 400 µl 2 % CTAB lysis buffer in 1.5 micro- included selective antibiotic-amended media [1 % tubes. Tubes were frozen overnight at –20 °C and Streptomycin (Sigma) and 2 % Cycloheximide then the tissue samples were ground using a plastic (Acros Organics)] that allowed the near-exclusive blue pestle. After this, the tubes were incubated in a growth of resistant blue-stain species. After becom- 65 °C water bath for two hours. The samples were 2 Sydowia 70 (2018) Mercado & Ortiz-Santana: Beetle mutualist Leptographium longiclavatum Fig. 1. Study site (star) in the Roosevelt National Forest (gray polygon). The forest is part of the southern Rocky Mountains. – Fig. 2. Affected forest hectares in Larimer County, Colorado from 2009 to 2013 by Mountain pine beetle relates directly to the insect’ population level which was receding during the study. Most of this insect’s activity in this county was located within the Roosevelt National Forest. Data adapted from USDA/Forest Health and Technologies. then centrifuged at 13000 rcf for 6 min at room tem- other sequences available in GenBank (Benson et al. perature (RT) and 300 µl of supernatant were trans- 2013) via BLASTn search. Ten new ITS2-LSU and ferred to a new tube. Next, 350 µl of cold 2-propanol β-tubulin sequences were generated, and 27 se- was added to each tube and placed at –80 °C for quences pertaining to the genera Leptographium 15 min.
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